Nematode Parasites of Brazilian Piciformes Birds: a General Survey with Description of Procyrnea Anterovulvata N
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Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 91(4): 479-487, Jul./Aug. 1996 479 Nematode Parasites of Brazilian Piciformes Birds: a General Survey with Description of Procyrnea anterovulvata n. sp. (Habronematoidea, Habronematidae) Roberto Magalhães Pinto+, J Júlio Vicente, Dely Noronha Laboratório de Helmintos Parasitos de Vertebrados, Instituto Oswaldo Cruz, Av. Brasil 4365, 21045-900 Rio de Janeiro, RJ, Brasil Thirty species of nematodes recovered from Piciformes hosts are reported. Procyrnea anterovulvata n. sp. from Chelidoptera tenebrosa brasiliensis is described and compared to P. colaptes and P. pileata. The considered morphometric parameters are mainly related to the ratio between length of the body/ distance of the vulva to the anterior end. It is approximately 1:0.5 in P. colaptes and P. pileata compared to 1:0.1 in the new species. The male of Synhimantus (Dispharynx) crassissima is described for the first time. Thelazia ( Thelaziella) spizaeti is revalidated and new records are reported for some species. Key words: nematodes - Procyrnea anterovulvata n. sp. - new records - Piciformes - birds - Brazil The nematodes identified during the present in- tracheolopyrus (Malherbe); 1 Picumnus cirratus vestigation parasitize a great number of hosts, dis- maconelli Sharpe. RAMPHASTIDAE: 3 tributed in four families of Piciformes birds. Pteroglossus aracari aracari L.; 3 Ramphastos This survey was scheduled to provide further tucanus tucanus L. data on morphometrics, host records and geo- Nematodes were preserved in Railliet & graphical distribution for the nematode parasites Henry’s solution (0.85% NaCl solution: 93 ml; of jacamars, puffbirds, toucans and woodpeckers formaldehyde: 5 ml; glacial acetic acid: 2 ml) and in Brazil. were processed for study as described elsewhere MATERIALS AND METHODS (Pinto et al. 1993). Preparation of “en face” mounts was done ac- Seventy-four samples of nematodes, recovered cording to Anderson (1958). Illustrations were pre- between 1913 and 1963 in Brazilian North, Cen- pared with a drawing tube connected to an Olympus tral and Southeastern regions during institutional light microcope. Measurements are in microme- scientific expeditions and deposited in the ters, unless otherwise indicated. NHR and NGD Helminthological Collection of the Oswaldo Cruz indicate New Host Record and New Geographical Institute (CHIOC), were studied. The number of Distribution, respectively. Classification of the examined specimens, according to host family is: nematodes follow Anderson and Bain (1976), BUCCONIDAE: 6 Chelidoptera tenebrosa Chabaud (1975 a, b, 1978) and confirmation of the brasiliensis Sclater; 3 Monasa nigrifrons taxonomic status of the hosts was based on Pinto nigrifrons (Spix); 5 Notharchus macrorhynchos (1978) and Sick (1984). swainsoni (G. R. Gray); 1 Nystalus chacuru chacuru (Vieillot); 11 Nystalus maculatus RESULTS maculatus (Gmelin). GALBULIDAE: 2 Galbula (Habronematoidea, Habronematidae, ruficauda rufoviridis Cabanis. PICIDAE: 15 Celeus Habronematinae) flavescens flavescens (Gmelin); 11 Celeus Procyrnea anterovulvata n. sp. flavescens lugubris (Malherbe); 2 Celeus jumana ( Fig. 1 a-f ) jumana (Spix); 6 Phloeoceastes melanoleucos Description: morphometrics based on five melanoleucos (Gmelin); 3 Phloeoceastes robustus specimens, two males and three females. (Lichtenstein); 1 Phloeoceastes rubricollis Males (Fig. 1 d, e): body 4.99-5.18 mm long, 150-160 wide. Mouth with two lips with three pedunculate papillae each, two small, lateral in the outer circle and one large, central in the inner; two interlabia present. Oral aperture nearly round. Buc- +CNPq research fellow Proc. no. 300374/80-1. Fax: 55- 21-260.4866 cal capsule with thick sclerotized lining, 32-39 Received 7 November 1995 long. Muscular and glandular esophagus 300-320 Accepted 6 May 1996 and 1.58-1.63 mm long, respectively. Nerve ring 480 Nematode Parasites of Brazilian Piciformes Birds RM Pinto et al. Fig. 1: Procyrnea anterovulvata n. sp. – a: anterior portion of female, ventral view. b: anterior extremity of female, lateral view. c: head of female, en face view. d: posterior extremity of male, ventral view. e: posterior portion of male, ventro-lateral view. f: posterior extremity of female, lateral view. Bars: 0.02 mm in Fig. c; 0.1 mm in Figs b, d, f; 0.2 mm in Fig. e; 0.5 mm in Fig. a. 180 from anterior extremity. Excretory pore not absent. Eleven pairs of pedunculate caudal papil- observed. Left spicule slender, 1.56-1.62 mm long. lae, of which four pairs are pre- and seven post- Right spicule stouter, 240-270 long. Gubernaculum cloacal, supported by large and prominent caudal Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 91(4), Jul./Aug. 1996 481 alae. Cloacal aperture 110-130 from posterior ex- (Acuarioidea, Acuariidae, Acuariinae) tremity. Synhimantus (Dispharynx) crassissima (Molin, Females (Fig. 1 a, b, c, f ): body 12.24-12.75 1860) Chabaud, 1975 mm long, 220-260 wide. Mouth and buccal cap- ( Fig. 2 a-c ) sule as in males; buccal capsule 39-46 long. Mus- Morphometrics: based on seven specimens, cular and glandular esophagus 320-340 and 2.03- four males and three females, recovered from 2.17 mm long, respectively. Nerve ring 180 from Ramphastos t. tucanus. anterior extremity. Excretory pore not observed. Description: males (Fig. 2 b ): body 6.51-8.62 Vulva 1.68-1.96 mm from anterior extremity. Va- mm long, 220-300 wide. Mouth with two large gina 1.54-1.68 mm long. Eggs 50-54 long, 28-32 papilliform lips. Oral aperture oval-elongate, near wide. Anus 120-130 from posterior extremity. of which derives two pairs of cephalic cordons. Taxonomic summary Buccal capsule 120-170 long. Cephalic cordons thick, markedly flexed, strongly recurrent, not anas- Type host: Chelidoptera tenebrosa brasiliensis; tomosing, 730-770 long. Muscular and glandular common name: swallow-wing (“andorinha, miolinho, urubuzinho”) esophagus 680-720 and 2.03-2.45 mm long, re- spectively. Nerve ring 280-300 from anterior ex- Site of infection: gizzard tremity. Excretory pore not observed. Left spicule Type locality: Conceição da Barra, State of Espírito Santo, Brazil slender, 460-500 long. Right spicule stouter, 190- 210 long. Gubernaculum absent. Ten pairs of Specimens studied: CHIOC no. 32,783 d (alotype), pedunculate caudal papillae, of which four are pre- 32,783 a (holotype), 32,783 b, c, e, f (paratypes) (whole mounts); 14,811 (wet material). and six post-cloacal, supported by narrow caudal alae. Cloacal aperture 210-270 from posterior ex- Etymology: the specific name derives from the tremity. Latin anterior + vulva, meaning “which posseses the vulva in the anterior portion of the body”. Redescription: females (Fig. 2 a, c): body 7.65- 9.53 mm long, 570-580 wide. Mouth and oral ap- Remarks erture as referred for the males. Buccal capsule 140- The species of Procyrnea Chabaud, 1975 180 long. Cephalic cordons as referred for the present the vulvar aperture in the middle portion males, 680 long. Muscular and glandular esopha- of the body (Chabaud 1958), slightly pre- or post- gus 510-680 and 1.96-2.38 mm long, respectively. equatorial. Nevertheless, the ratio between length Nerve ring 280-300 from anterior extremity. Ex- of the body/distance of vulva to the anterior end is cretory pore not observed. Vulva in posterior part approximately 1:0.5 in all previously described spe- of the body, 570-930 from posterior extremity. cies of the genus. Ovijector 210 long. Eggs 39-43 long, 25-28 wide. According to Chabaud and Brygoo (1958), two Anus 120-160 from posterior extremity. species of Procyrnea parasitize Piciformes hosts: P. colaptes (Walton, 1923) Chabaud, 1975, in Taxonomic summary which the above mentioned ratio is of 1:0.49-0.58 Hosts: Chelidoptera tenebrosa brasiliensis NHR; (present data) and P. pileata (Walton, 1928) Notharchus macrorhynchus swainsoni (= Bucco Chabaud, 1975 with ratio of 1:0.47-0.59 (Walton swainsoni); common name: spotted puffbird 1928). Both species are reported from USA, para- (“macuru”) - NHR; Ramphastos t. tucanus (= sitizing Colaptes auratus luteus Bangs and Ramphastos monilis); common name: red-billed Hylotomus pileatus, respectively (Walton 1923, toucan (“tucano de peito branco, quirina, pia- 1928, Cram 1927). pouco”) - NHR Procyrnea anterovulvata n. sp. is compared to Other Piciformes host: Ramphastos vitellinus these two species based on the high specificity of Lichtenstein, according to Cram (1927) this group of nematodes to this order of birds. In Site of infection: gizzard the new species the ratio between lenght of body/ Localities: Angra dos Reis, State of Rio de Janeiro; distance of the vulva to the anterior end is of Belém, State of Pará; and Engano, State of Espírito 1:0.13-0.15, clearly distinguishing P. anterovulvata Santo, Brazil n. sp. from P. colaptes and P. pileata, as well as Specimens studied: CHIOC no. 32,778, 32,779 a- from the other species actually included in the ge- b, 32,780 a-h (whole mounts). nus. Moreover, the right spicule in males of P. Remarks anterovulvata n. sp. is remarkably shorter (240- This species was originally described as 270) in comparison with the observed in P. Dispharagus crassissimus in 1860 from a Brazil- colaptes and P. pileata (390-410 and 440, re- ian toucan based on female specimens and was spectively). redescribed by Cram (1927) as Dispharynx 482 Nematode Parasites of Brazilian Piciformes Birds RM Pinto et al. crassissima also considering female specimens (Thelazioidea, Thelaziidae, Thelaziinae) only. Males were referred as “unknown” by both Thelazia (Thelaziella) spizaeti Strachan, 1957 authors. The present data refer to the first descrip- (Fig. 2 d-f) tion of male of this species. Taxonomic summary (Seuratoidea, Seuratidae, Seuratinae) Host: Pteroglossus a. aracari; common name: Skrjabinura spiralis Gnédina, 1933 black-necked aracari (“araçari”) - NHR Taxonomic summary Site of infection: orbital cavity Host: Galbula ruficauda rufoviridis; common Locality: Raul Soares, State of Minas Gerais, Bra- zil name: rufous-tailed jacamar (“beija-flor grande, Specimens studied: CHIOC no. 32,782 a-c (whole cuitelão”) - NHR Site of infection: intestine mounts).